APOE genotype alters glial activation and loss of synaptic markers in mice
Open accessAbstract
The ϵ4 allele of the Apolipoprotein E (APOE) gene is the strongest genetic risk factor for late‐onset Alzheimer's disease (AD), and affects clinical outcomes of chronic and acute brain damages. The mechanisms by which apoE affect diverse diseases and disorders may involve modulation of the glial response to various types of brain damage. We examined glial activation in a mouse model where each of the human APOE alleles are expressed under the endogenous mouse APOE promoter, as well as in APOE knock‐out mice. APOE4 mice displayed increased glial activation in response to intracerebroventricular lipopolysaccharide (LPS) compared to APOE2 and APOE3 mice by several measures. There were higher levels of microglia/macrophage, astrocytes, and invading T‐cells after LPS injection in APOE4 mice. APOE4 mice also displayed greater and more prolonged increases of cytokines (IL‐1β, IL‐6, TNF‐α) than APOE2 and APOE3 mice. We found that APOE4 mice had greater synaptic protein loss after LPS injection, as measured by three markers: PSD‐95, drebin, and synaptophysin. In all assays, APOE knock‐out mice responded similar to APOE4 mice, suggesting that the apoE4 protein may lack anti‐inflammatory characteristics of apoE2 and apoE3. Together, these findings demonstrate that APOE4 predisposes to inflammation, which could contribute to its association with Alzheimer's disease and other disorders. © 2012 Wiley Periodicals, Inc.
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Previous studies utilizing intracerebroventricular LPS injections have demonstrated significant increases in pro-inflammatory cytokines (IL1β, IL6, TNFα), particularly in APOE4 mice.
“Previous studies utilizing intracerebroventricular LPS injections have demonstrated significant increases in pro-inflammatory cytokines (IL1β, IL6, TNFα), particularly in APOE4 mice [78].”
ApoE4-expressing mice exhibit higher levels of glial activation, cytokine production and synaptic marker loss after LPS challenge compared to apoE2- and apoE3-expressing mice.
“apoE4-expressing mice exhibit higher levels of glial activation, cytokine production and synaptic marker loss after the inflammatory challenge with lipopolysaccharide (LPS) when compared to apoE2- and apoE3-expressing mice”
From ApoE4 reduction: An emerging and promising therapeutic strategy for Alzheimer's disease (2022) · cites this paper as Zhu et al 2012
ApoE4 mice and Alzheimer's disease brains show dysfunctional neurons and activated astrocytes.
“This is consistent with dysfunctional neurons and activated astrocytes seen in both ApoE4 mice (Zhu et al., 2012) and AD brains (Long and Holtzman, 2019).”
From ApoE4 Impairs Neuron-Astrocyte Coupling of Fatty Acid Metabolism (2021) · cites this paper as Zhu et al., 2012
Several in vivo studies of E4 mice and humans show an exaggerated response to inflammation in E4 individuals.
“several in vivo studies of E4 mice and humans show an exaggerated response to inflammation in E4 individuals (Vitek et al., 2009; Shi et al., 2017; Zhu et al., 2012; Gale et al., 2014).”
From APOE4 reshapes the lipid droplet proteome and modulates microglial inflammatory responses (2025) · cites this paper as Zhu et al., 2012
Intracerebroventricular administration of LPS induces greater glial activation and cytokine secretion in E4 mice than in E2 or E3 mice at 72 hours post-injection.
“Intracerebroventricular administration of LPS has been shown to induce greater glial activation and cytokine secretion in E4 mice than in E2 or E3 mice at 72 hours post-injection”
From Older adult APOE4 mice exhibit modest immunometabolic adaptation following microglial APOE2 replacement (2027) · cites this paper as Zhu et al., 2012
ApoE4 produces the strongest glial activation.
“with ApoE4 causing the greatest activation [97]”
From ApoE, ApoE Receptors, and the Synapse in Alzheimer's Disease (2017) · cites this paper as [97]
Glial activation is influenced by ApoE isoform.
“glial activation is affected by ApoE isoform”
From ApoE, ApoE Receptors, and the Synapse in Alzheimer's Disease (2017) · cites this paper as [97]
Peripheral endotoxin can cause microglial activation and loss of brain synapses, and the endotoxin-binding protein APOE2 can protect against this synaptic loss.
“Peripheral endotoxin can also cause microglial activation and loss of brain synapses, and the endotoxin-binding protein APOE2 can protect against this synaptic loss [64].”
From The endotoxin hypothesis of neurodegeneration (2019) · cites this paper as [64]
A greater immune response associated with the ε4 allele is also observed in human APOE-TR mice and in cultured microglia/macrophages upon LPS stimulation.
“A greater immune response associated with the ε4 allele is also observed in human ApoE-targeted replacement (APOE-TR) mice [G] and in cultured microglia/macrophages upon LPS stimulation108–110.”
From Interplay between innate immunity and Alzheimer disease: APOE and TREM2 in the spotlight (2018) · cites this paper as [110]
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Human APOE4 increases microglia reactivity at Aβ plaques in a mouse model of Aβ deposition
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“When discussing effects of ApoE receptor signaling on the astrocyte, it is important to point out that glial activation is affected by ApoE isoform, with ApoE4 causing the greatest activation [97].”
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Reduction in DHA transport to the brain of mice expressing human APOE 4 compared to APOE 2
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Murine Gut Microbiome Association With APOE Alleles
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Self-citation
- Authors
- Zhu, Y., Nwabuisi‐Heath, E., Dumanis, S. B., Tai, L. M., Yu, C., Rebeck, G. W., & Ladu, M. J.
- Affiliations
- Fujian Medical University (CN)
- University of Illinois Chicago (US)
- Georgetown University (US)
- Corresponding author
- Ladu, Mary Jo
- Venue
- Glia
- Publisher
- Wiley
- Published
- 2012-01-06
- Volume
- 60
- Issue
- 4
- Pages
- 559-569
- ISSN
- 0894-1491 (ISSN-L)
- 1098-1136
- PMC
- PMC3276698
- OpenAlex
- W2127101809
- Cited by
- 224
- References
- 54
- Citations by year
- 2026: 12 · 2025: 16 · 2024: 14 · 2023: 20 · 2022: 25 · 2021: 29 · 2020: 21 · 2019: 20 · 2018: 8 · 2017: 10 · 2016: 9 · 2015: 12 · 2014: 13 · 2013: 12 · 2012: 3
- FWCI
- 6.44
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Glia (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- University of Illinois at Chicago
- National Institute on Aging (P01AG030128)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- APOE ε4, apolipoprotein E, glial activation, neuroinflammation, lipopolysaccharide, microglia, astrocytes, T cell infiltration, cytokines, PSD-95, synaptophysin, Alzheimer's disease risk
- MeSH terms
- Disks Large Homolog 4 Protein, Analysis of Variance, Animals, Antigens, Differentiation, Apolipoproteins E, Brain, Enzyme-Linked Immunosorbent Assay, Gene Expression Regulation, Genotype, Glial Fibrillary Acidic Protein, Humans, Injections, Intraventricular, Lipopolysaccharides, Membrane Proteins, Mice, Transgenic, Neuroglia, Synapses, Cytokines, Mice, Guanylate Kinases, Apolipoprotein E3, Apolipoprotein E4, Apolipoprotein E2
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